Document Type : Articles

Authors

1 General Directorate of Agriculture in Sulaimani. Ministry of Agricultural and Water Resources, Sulaimani, Kurdistan Region, Iraq

2 Dept. of Horticulture, College of Agriculture, University of Sulaimanie, Kurdistan Region- Iraq

Abstract

Fruit samples of strawberry were collected from local markets in Sulaimani Governorate/Iraq which they are imported from Turkey and Iran.Two different methods for identifying the fungi were used; morphologically, depending on some characteristic such as the shape of the spores, the color and the general shape of the fungus. Also to confirm the diagnosis fungal, molecular method was used. The mycotic observations showed that there were nine distinct fungi. The molecular data was blasted at NCBI checked and the identification rate was between 97-100%. The diagnosed fungi were (Alternaria alternate, Aspergillus niger, Botrytis cinerea, Cladosporium cladosporioides, Fusarium oxysporum f. sp. fragariae, Nigrospora sphaerica, Penicillium raistrickii, Penicillium griseofulvum and Rhizopus stolonifer). The highest infestation percent was recorded for A. niger 26.02%, while the lowest was for Fusarium oxysporum f. sp. fragariae 1.08%, pathogenicity test was performed for the isolated fungi and revealed that all of the fungi were pathogenic more than 90%. Samples from local markets showed no significant differences in disease incidence and the severity of the disease. For management of the fungi associated with strawberries, different method have been used in vitro (rosemary and pomegranate) plant extracts, salicylic acid (SA), potassium metabisulphite (KMS) and two fungicides. 1% and 2% rosemary plant extracts gave the highest inhibition of (P. griseofulvum) also, pomegranate peel extract 4% had a significant effect on (N. sphaerica). In addition SA were effective on all fungi and KMS had the same as the fungi excepted (R. stolonifera) compared to control treatment.

Keywords

  1. Abdelkader, M., Ahcen, B., Rachid, D. and Hakim, H. (2014) 'Phytochemical study and biological activity of sage (Salvia officinalis L.)', Int. J. Bioeng., Life. Sci., 8(11): 1253-1257.
  2. Addinsoft (2016). XLSTAT 2016: Data analysis and statistical solution for Microsoft Excel. Paris: Pentraeth, https://www.xlstat.com.
  3. Adeoye, I. B., Odeleye, O. M. O., Babalola, S.O. and Afolayan, S. O. (2009) 'Economic analysis of tomato losses in Ibadan metropolis, Oyo State, Nigeria', Afr. J. Basic & Appl. Sci., 1(5-6): 87-92.
  4. Ajanal, M., Gundkalle, M. B. and Nayak, S. U. (2012) 'Estimation of total alkaloid in Chitrakadivati by UV-Spectrophotometer', Anc. Sci. Life, 31(4): 198-201.
  5. Al-Rawi, K. and Khalafullah, A. (1980) Design and Analysis of Agricultural Experiments. Iraq: Dar Al Kutb for Printing and Publishing - University of Mosul, p. 488.
  6. Amal, S.A., El-Mogy, M. M., Aboul-Anean, H.E. and Alsanius, B.W. (2010) 'Improving strawberry fruit storability by edible coating as a carrier of thymol or calcium chloride', J. Hort. Sci. Ornam. Plants, 2(3): 88-97.
  7. Angioni, A., Barra, A., Cereti, E., Barile, D., Coïsson, J. D., Dessi, Arlorio, M.,Dessi, S., Coroneo, V. and Cabras, P. (2004) 'Chemical composition, plant genetic differences, antimicrobial and antifungal activity investigation of the essential oil of Rosmarinus officinalis L', J. Agr. Food chem., 52(11): 3530-3535.
  8. Avenot, H., Morgan, D. P. and Michailides, T. J. (2008) 'Resistance to pyraclostrobin, boscalid and multiple resistance to Pristine®(pyraclostrobin+ boscalid) fungicide in Alternaria alternata causing alternaria late blight of pistachios in California', Plant pathol., 57: 135-140.
  9. Baba, S. A. and Malik, S. A. (2015) 'Determination of total phenolic and flavonoid content, antimicrobial and antioxidant activity of a root extract of Arisaema jacquemontii Blume', J. Taibah Uni. Sci., 9(4): 449-454.
  10. Balakrishnan, A. and Kokilavani, R. (2012) 'Influence of Cucumis Trigonus fruit extract on biochemical parameters in Urolithiasis induced Wistar albino rats', Elixir Appl. Bot., 42: 6209-6212.
  11. Banani, H., Marcet-Houben, M., Ballester, A.-R., Abbruscato, P., Gonzalez-Candelas, L., Gabaldon, T. and Spadaro, D. (2016) 'Genome sequencing and secondary metabolism of the postharvest pathogen Penicillium griseofulvum', BMC Genomics, 17(19): 1-14.
  12. Barnett, H. L. and Hunter, B. B. (1999) Illustrated genera of imperfect fungi (4th Eds.), Burgess. Minneapolis, Minnesota: APS Press, p. 218.
  13. Behr, M., Legay, S. and Evers, D. (2013) 'Molecular identification of Botrytis cinerea, Penicillium spp. and Cladosporium spp. in Luxembourg', J. Int. des Sci. de la vigne et du vin, 47(4), pp. 239-247.
  14. Bensch, K., Braun, U., Groenewald, J. Z. and Crous, P. W. (2012) The genus cladosporium ( 4th Eds), Elsevier Stud. Mycol., 72(1): 1-401.
  15. Bowers, J. H. and Locke, J. C. (2000) 'Effect of botanical extracts on the population density of Fusarium oxysporum in soil and control of Fusarium wilt in the greenhouse', Plant disease, 84(3): 300-305.
  16. Buyukbay, E. O., Uzunoz, M. and Bal, H. S. G. (2011) 'Post-harvest losses in tomato and fresh bean production in Tokat province of Turkey', Sci. Res. Essays, 6(7): 1656-1666.
  17. Chliyeh, M., Achbani, E., Rhimini, Y., Selmaoui, K., Touhami, A. O., Filali-Maltouf, A., El Modafar, C., Moukhli, A., Oukabli, A., Benkirane, R. and Douira, A. (2014) 'Pathogenicity of four fungal species on fruits and leaves of the olive tree (Olea europaea L.)', Int. J. Pure & Appl. Biosci., 2(4): 1-9.
  18. Dahham, S. S., Ali, M. N., Tabassum, H. and Khan, M. (2010) 'Studies on antibacterial and antifungal activity of pomegranate (Punica granatum L.)', American Eurasian J. Agric. Environ. Sci., 9(3): 273-281.
  19. Devkota, A. R., Dhakal, D. D., Gautam, D. M. and Dutta, J. P. (2014) 'Assessment of fruit and vegetable losses at major wholesale markets in Nepal', Int. J. Appl. Sci. Biotechnol., 2(4): 559-562.
  20. Dixit, S. N., Tripathi, S.C. and Upadhyay, R. R. (1976) 'The antifungal substance of rose flowers (Rosa indica)', Eco. Bot., 30(4): 371-374.
  21. Elad, Y., Williamson, B., Tudzynski, P. and Delen, N. (2007) Botrytis: biology, pathology and control. ( 1st Eds.), Springer, p. 428.
  22. Elfalleh, W., Hannachi, H., Tlili, N., Yahia, Y., Nasri, N. and Ferchichi, A. (2012) 'Total phenolic contents and antioxidant activities of pomegranate peel, seed, leaf and flower', J. Med. Plant Res., 6(32): 4724-4730.
  23. Ellis, C., Karafyllidis, I. and Turner, J. G. (2002) 'Constitutive activation of jasmonate signaling in an Arabidopsis mutant correlates with enhanced resistance to Erysiphe cichoracearum, Pseudomonas syringae, and Myzus persicae', Mol. Plant-Microbe Interact., 15(10): 1025-1030.
  24. Embaby, E. M., Mona, M. A. and Aiat, N. M. (2016) 'Control strawberry fruit decay caused by some mold fungi', Int. J. Pharm. Tech. Res., 9(10): 184-193.
  25. Endo, E. H., Cortez, D. A. G., Ueda-Nakamura, T., Nakamura, T., Nakamura, C. V. and Dias Filho, B. P. (2010) 'Potent antifungal activity of extracts and pure compound isolated from pomegranate peels and synergism with fluconazole against Candida albicans', Res. Microbiol., 161(7): 534-540.
  26. Erkan, N., Ayranci, G. and Ayranci, E. (2008) 'Antioxidant activities of rosemary (Rosmarinus Officinalis L.) extract, blackseed (Nigella sativa L.) essential oil, carnosic acid, rosmarinic acid and sesamol', Food chem., 110(1): 76-82.
  27. Eshghi, S., Abdi, G., Tafazoli, E. and Yavari, S. (2007) 'Strawberry research and biotechnology in Iran', Middle Eastern & Russian J. Plant Sci. Biotech., 1(2): 39-41.
  28. Feliziani, E. and Romanazzi, G. (2016) 'Postharvest decay of strawberry fruit: Etiology, epidemiology, and disease management', J. Berry Res., 6(1): 47-63.
  29. Genena, A. K., Hense, H., Smânia Junior, A. and Souza, S. M. d. (2008) 'Rosemary (Rosmarinus officinalis): a study of the composition, antioxidant and antimicrobial activities of extracts obtained with supercritical carbon dioxide', Ciênc. Tecnol. Aliment., Campina, 28(2): 463-469.
  30. Gudmestad, N. C., Arabiat, S., Miller, J. S. and Pasche, J. S. (2013) 'Prevalence and impact of SDHI fungicide resistance in Alternaria solani', Plant Disease, 97(7): 952-960.
  31. Hassan, M., Farooq, M. and Gul, F. (2014) 'In vitro evaluation of some fungicides against common fungal pathogen of early blight and fruit rot of tomatoes', J. Appl. Environ. Biol. Sci, 4(9S): 424-429.
  32. Hcini, K., Sotomayor, J., Jordan, M. J. and Bouzid, S. (2013) 'Chemical composition of the essential oil of Rosemary (Rosmarinus officinalis L.) of Tunisian origin', Asian J. Chem., 25(5): 2601-2603.
  33. Seeram, N. P., Schulman, R. N. and Heber, D. (2006) Pomegranates: ancient roots to modern medicine. ( 1st Eds.), CRC press, p. 262.
  34. Henry, T., Iwen, P. C. and Hinrichs, S. H. (2000) 'Identification of Aspergillus species using internal transcribed spacer regions 1 and 2', J. Clin. Microbiol., 38(4): 1510-1515.
  35. Husaini, A. M. and Neri, D. (2016) 'Strawberry: growth, development and diseases'. ( 1st Eds.), London, UK: CABI, pp. 157-195.
  36. Ismael, J. H. S. and Mahmmod, S. H. (2018) 'Diagnosis and in vitro control of tomato leaf spot caused by Alternaria alternata in Sulaimani governorate', JZS (A) Pure & Appl. Sci., 20: 637-650.
  37. Ismael, J. H. and Mahmoodd, S. H. (2016) 'Management of tomato damping-off using natural plant extracts, Trichoderma harzianum and selected fungicides in Penjween, Sulaimani governorate, kurdistan, Iraq', Malays Appl Biol, 45(1): 35-48.
  38. Javeed, S. Z. and Fatima, S. (2017) 'Album-post harvest diseases of fruit : Epitome', Int. J. Multidiscip. Res. Dev., 4(4): 42-51.
  39. Jyoti, K. (2015) Effect of postharvest treatments on storage quality of bell pepper (Capsicum annum). Master of science, Dr Yashwant Singh Parmar University of Horticulture and Forestry, Nauni Solan 173 230 (HP), INDIA- College of Horticulture.
  40. Kayraldiz, A., Kaya, F. F., Canimoĝlu, S. and Rencüzoĝullari, E. (2006) 'Mutagenicity of five food additives in Ames/Salmonella/microsome test', Ann. Microbiol., 56(2): 129-133.
  41. Kortei, N., Odamtten, G., Obodai, M., Appiah, V. and Wiafe-Kwagyan, M. (2015) 'Evaluating the effect of gamma irradiation and steam sterilization on the survival and growth of composted sawdust fungi in Ghana', British Microbiol. Res. J., 7(4): 180-192.
  42. Lattanzio, V., Lattanzio, V. M. T. and Cardinali, A. (2006) 'Role of phenolics in the resistance mechanisms of plants against fungal pathogens and insects', Phytochem. Adv. Res.,37/ 661(2): 23-67.
  43. Li, Y., Guo, C., Yang, J., Wei, J., Xu, J. and Cheng, S. (2006) 'Evaluation of antioxidant properties of pomegranate peel extract in comparison with pomegranate pulp extract', Food Chem., 96(2): 254-260.
  44. Maas, J. L. (2004) 'Strawberry disease management. In: Naqvi S.A. M.H. (1st Eds) Disease of fruits and vegetables: Volume II: Springer, Dordrecht.
  45. Mahmmod, S. H. and Ismael, J. H. S. (2020) ' Effect of some botanical fungicide and chemicals as forest seed dressing on quality of the seeds, 11(10): 485-488.
  46. McKinney, H. (1923) 'Influence of soil, temperature and moisture on infection of wheat seedlings by Helminthosporium sativum', J. Agri. Res., 26: 195–218.
  47. Mohammadi, A. and Bahramikia, S. (2019) 'Molecular identification and genetic variation of Alternaria species isolated from tomatoes using ITS1 sequencing and inter simple sequence repeat methods', Curr. Med. Mycol., 5(2): 1-8.
  48. Morsy, A., Abd-Alla, M. and Abd-El-Kareem, F. (1999) 'Evaluation of chitosan as a substitute of fungicides for postharvest disease control: Strawberry decay', Egypt J. Phytopathol, 27(2): 109-116.
  49. Mradu, G., Saumyakanti, S., Sohini, M. and Arup, M. (2012) 'HPLC profiles of standard phenolic compounds present in medicinal plants', Int. J. Pharmacog. Phytochem. Res., 4(3): 162-167.
  50. Myresiotis, C., Bardas, G. A. and Karaoglanidis, G.S. (2008) 'Baseline sensitivity of Botrytis cinerea to pyraclostrobin and boscalid and control of anilinopyrimidine-and benzimidazole-resistant strains by these fungicides', Plant disease, 92(10): 1427-1431.
  51. Nashwa, S. M. and Abo-Elyousr, K. A. (2012) 'Evaluation of various plant extracts against the early blight disease of tomato plants under greenhouse and field conditions', Plant Protect. Sci., 48(2): 74-79.
  52. Niu, C., Kebede, H., Auld, D. L., Woodward, J. E., Burow, G. and Wright, R. J. (2008) 'A safe inexpensive method to isolate high quality plant and fungal DNA in an open laboratory environment', Afr. J. Biotechnol., 7(16): 2818-2822.
  53. Nunes, C. A. (2012) 'Biological control of postharvest diseases of fruit', Eur. J. Plant Pathol., 133(1): 181-196.
  54. Olivier, C., MacNeil, C. R. and Loria, R. (1999) 'Application of organic and inorganic salts to field-grown potato tubers can suppress silver scurf during potato storage', Plant disease, 83(9): 814-818.
  55. Orak, H. H., Demirci, A. Ş. and Gümüş, T. (2011) 'Antibacterial and antifungal activity of pomegranate (Punica granatum L. cv.) peel', Elec. J. Environ., Agri. Food Chem., 10(3): 1958-1969.
  56. Pande, G. and Akoh, C. C. (2009) 'Antioxidant capacity and lipid characterization of six Georgia-grown pomegranate cultivars', J. Agric. Food Chem., 57(20): 9427-9436.
  57. Patil, J. S. and Suryawanshi, N. S. (2014) 'Fruit rot of strawberry caused by Alternaria alternata control using homoeopathic medicines', Int. J. Pharm. Sci. Invent., 3(11): 57-58.
  58. Pitt, J. I. and Hocking, A. D. (2009) Fungi and food spoilage. (3rd Eds.), New York: Springer, p. 388.
  59. Potter, D., Eriksson, T., Evans, R. C., Oh, S., Smedmark, J., Morgan, D. R., Kerr, M., Robertson, K. R., Arsenault, M., Dickinson, T. A. and Campbell, C. S. (2007) 'Phylogeny and classification of Rosaceae', Plant Syst. Evol., 266(1-2):5-43.
  60. Pour, A. R., Mirzargar, S. S., Soltani, M., Mousavi, H. A. E. and Seyed, A. (2014) 'The antibacterial effects of Cuminum cyminum L. and Rosmarinus officinalis extracts and essential oil against Lactococcus garvieae in laboratory conditions on rainbow trout', Eur. J. Exp. Biol., 4(1): 456-463.
  61. Qin, X., Xiao, H., Xue, C., Yu, Z., Yang, R., Cai, Z. and Si, L. (2015) 'Biocontrol of gray mold in grapes with the yeast Hanseniaspora uvarum alone and in combination with salicylic acid or sodium bicarbonate', Postharvest Biol. Technol., 100: 160-167.
  62. Romanazzi, G., Feliziani, E., Santini, M. and Landi, L. (2013) 'Effectiveness of postharvest treatment with chitosan and other resistance inducers in the control of storage decay of strawberry', Postharvest Biol. Techno., 75: 24-27.
  63. Rongai, D., Pulcini, P., Lernia, G. D., Nota, P., Preka, P. and Milano, F. (2019) 'Punicalagin content and antifungal activity of different pomegranate (Punica ganatum L.) genotypes', Hortic., 5(52): 1-9.
  64. Salami, P., Ahmadi, H., Keyhani, A. and Sarsaifee, M. (2010) 'Strawberry post-harvest energy losses in Iran', Researcher, 2(4): 67-73.
  65. Sastry, A. S. and Bhat, S. (2018) Essentials of medical microbiology. (2nd Eds.), NewDeihi, India: Jaypee Brothers Medical Ltd, p. 692.
  66. Sethi, S. (2007) 'Horticulture-Post Harvest Technology, Principles of Food Processing', Indian Agriculture Research Institute, New Delhi. Mohammad Rais, Shatroopa Acharya and Neeraj Sharma, p. 479.
  67. Singha, I. M., Kakoty, Y., Unni, B. G., Das, J. and Kalita, M. C. (2016) 'Identification and characterization of Fusarium sp. using ITS and RAPD causing fusarium wilt of tomato isolated from Assam, North East India', J. Genet. Eng. Biotechnol., 14(1): 99-105.
  68. Smith, I. M., Dunez, J., Phillips, D., Lelliott, R. and Archer, S. (2009). European handbook of plant diseases (1st Eds.), London: John Wiley & Sons, p. 598.
  69. Stauct, G. (1989) 'The species of Fragaria, Their taxanomy and geographical distribution', Acta Hortic., 265: 23-34.
  70. Tofighi, Z., Ghazi, S. N., Hadjiakhoondi, A. and Yassa, N. (2016) 'Determination of cardiac glycosides and total phenols in different generations of Securigera securidaca suspension culture', Int. J. Pharmacog., 3(2): 25-31.
  71. Visagie, C. M., Houbraken, J., Frisvad, J. C., Hong, S.-B., Klaassen, C. H. W., Perrone, G., Seifert, K. A., Varga, J., Yaguchi, T. and Samson, R. A. (2014) 'Identification and nomenclature of the genus Penicillium', Stud Mycol., 78: 343-371.
  72. Wang, Y.-Y., Li, B.-Q., Qin, G.-Z., Li, L. and Tian, S.-P. (2011) 'Defense response of tomato fruit at different maturity stages to salicylic acid and ethephon', Sci. Hortic., 129(2): 183-188.
  73. Wheeler, B. E. J. (1969) An introduction to plant diseases, (Eds), John Wiley & Sons Ltd, London, New York, Sydney, Toronto, p. 374.
  74. White, T. J., Bruns, T., Lee, S. and Taylor, J. (1990) 'Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics', PCR protocols: a guide to methods and applications. (Eds), Academic Press, Inc., 18(1): 315-322.
  75. Woo, P. C., Leung, S.-Y., To, K. K., Chan, J. F., Ngan, A. H., Cheng, V. C., Lau, S. K. and Yuen, K.-Y. (2010) 'Internal transcribed spacer region sequence heterogeneity in Rhizopus microsporus: implications for molecular diagnosis in clinical microbiology laboratories', J. Clin. Microbiol., 48(1): 208-214.
  76. Zare, K., Nazemyeh, H., Lotfipour, F., Farabi, S., Ghiamirad, M. and Barzegari, A. (2014) 'Antibacterial activity and total phenolic content of the Onopordon acanthium L. seeds', Pharm. Sci., 20(1): 6-11.
  77. Zhang, H., Ma, L., Wang, L., Jiang, S., Dong, Y. and Zheng, X. (2008) 'Biocontrol of gray mold decay in peach fruit by integration of antagonistic yeast with salicylic acid and their effects on postharvest quality parameters', Biol. control, 47(1): 60-65.
  78. Zhang, S., Zheng, Q., Xu, B. and Liu, J. (2019) 'Identification of the fungal pathogens of postharvest disease on peach fruits and the control mechanisms of Bacillus subtilis JK-14', Toxins, 11(322): 1-15.
  79. Zhao, J., Zhang, Y., Wang, L., Wang, J. and Zhang, C. L. (2012) 'Bioactive secondary metabolites from Nigrospora sp. LLGLM003, an endophytic fungus of the medicinal plant Moringa oleifera Lam', World J. Microbiol. Biotechnol., 28(5): 2107-2112.